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Holgorsen spent time at Valdosta State (1993–95) as the quarterbacks, receivers and special teams coach under head coach Hal Mumme, at Mississippi College (1996–98) as the quarterbacks, receivers and special teams coach and at Wingate (1999) as the quarterbacks and receivers coach.

Holgorsen was a member of the coaching staff at Texas Tech from 2000–07, serving as the inside receivers coach from 2000–04, before being elevated to co-offensive coordinator alongside Sonny Dykes from 2005–06 and offensive coordinator in 2007. The move reunited him with head coach Mike Leach, whom Holgorsen had previously coached with at Valdosta State under Hal Mumme. While there, his offenses increased the amount of yardage from 324.8 yards of total offense to 529.6, an increase of more than 200 yards per game. The Red Raiders were No. 7 nationally prior to Holgorsen becoming offensive coordinator and raised their yardage total to No. 4 in 2005, his first season directing the offense. In his two years as offensive coordinator, his squad was nationally ranked No. 8 in 2006 and No. 3 in 2007. In 2007, Texas Tech led the nation in passing (470.31), was No. 2 in total offense (529.62) and was No. 7 in scoring offense (40.9). Quarterback Graham Harrell led the nation in total offense and Biletnikoff Award winner Michael Crabtree led the nation in receptions per game and receiving yards per game. In 2006, the Red Raiders ranked No. 3 nationally in passing offense and No. 6 in total offense. Harrell once again was outstanding, finishing No. 3 nationally in total offense with 344.38 yards per game. Texas Tech led the nation in passing in 2005, was No. 4 in scoring offense (39.4) and No. 6 in total offense (495.83). Quarterback Cody Hodges was No. 2 in the nation with 396.08 yards per game.

Houston has long been known for scoring a lot of points from the Veer that tallied 100 points in a single football game to the Run and Shoot of the late 1980s that re-wrote the college football record books. As the Offensive Coordinator at the University of Houston Dana Holgorsen gained prominence and recognition as one of the most promising, up-and-coming offensive coaches in the country and his success running the Cougar offense would set the table for future coaching opportunities. During his two-year tenure with the Cougars, Holgorsen's offenses posted earth-shattering numbers, accounting for 563 yards of total offense per game, passing for 433.7 yards per game and totaling more than 42.2 points per game. His offense ranked No. 3 in total offense in 2008 with a duo of freshmen quarterbacks and No. 1 in 2009 behind the arm of Heisman finalist and All-Conference quarterback Case Keenum. In 2008–2009, Quarterback Case Keenum, led the nation in total offense totaling 403.2 yards per game as a sophomore and 416.4 yards his junior season. He also ranked among the Top 10 nationally in pass efficiency both years.[4] Under Holgerson's tutelage Case Keenum would go on to become the all time leading passer in college football with more touchdowns than any quarterback in the history of college football. At Houston, Dana Holgorsen demonstrated his own brand of the Air Raid offense that often used motion to confuse opposing defenses, as well as wearing them down. In 2009, Holgorsen developed a set called the "diamond formation" which, features multiple diverging running backs in the backfield who adeptly use spread gain yards after catching short passes. Houston's extremely fast wide receivers were ideal to the style of spread Holgerson ran and Houston continued using much the same offense after Holgorsen departed to lead the NCAA with over 50 points per game, and 600 yards of offense per game in 2011. At Houston, Holgorsen not only mentored Case Keenum but offensive coaches including Kliff Klingsbury and Jason Phillips who continued running a Holgorsen-inspired Air Raid offense at Houston.

When Holgorsen was hired at Oklahoma State, the Cowboys' offense was ranked No. 61 nationally in total offense. In his first season the offense led the nation in total offense, averaging 537.6 yards per game, was No. 2 in passing offense, averaging 354.7 yards per game, and No. 3 in scoring offense, averaging 44.9 points per game.[5] The postseason accolades have been plentiful for Holgorsen's offensive players in 2010, quarterback Brandon Weeden became the first OSU passer to ever earn first team All-Big 12 honors. He was also a finalist for the Manning Award, given to the top quarterback in the nation. Wide receiver Justin Blackmon was named the recipient of the 2010 Biletnikoff Award, given to the top receiver in the nation, and running back Kendall Hunter was a finalist for the Doak Walker Award, given to the nation's top running back. Weeden, Hunter and Blackmon became only the second trio in NCAA history to pass for at least 3,000 yards, run for more than 1,500 yards and finish with more than 1,500 yards receiving in the same season.[4]

These are the school records set by the Dana Holgorsen-coordinated Oklahoma State Cowboys' offense during the 2010 season:[6]

On December 22, 2010; Holgorsen moved to West Virginia as offensive coordinator. At that time, athletic director Oliver Luck also announced that Holgorsen would replace Stewart as head coach in 2012, saying that he didn't think Stewart was capable of leading the Mountaineers to a national championship.[7]

The relationship between Stewart and Holgorsen was strained from the start and finally came to a head when Colin Dunlap, a former reporter from the Pittsburgh Post-Gazette, claimed Stewart had asked him and another reporter from the Charleston Gazette to dig up negative information about Holgorsen's behavior. Holgorsen did apologize for an early morning incident when he was asked to leave a West Virginia casino;[8] no further negative information came forth. While Luck was unable to fully substantiate the claims, he decided that Stewart had become too much of a distraction and forced Stewart to resign on June 10, naming Holgorsen head coach immediately.[9][10]

Luck had anticipated that the coach-in-waiting arrangement might not work as originally planned. Holgorsen's contract stated that his salary would be prorated at $1.4 million for the remainder of the season should he become head coach before 2012.[11] In addition, the $250,000 annual bonus applied to the head coaching salary would begin a year early, resulting in an additional $2 million over the six-year period addressed by his contract.[10]

Holgorsen coached the Mountaineers to a share of the Big East Conference crown in his first season at WVU and a Bowl Championship Series berth in the Orange Bowl, WVU's first appearance in the Orange Bowl. WVU defeated Clemson University 70–33 in that record-setting game.[12] The successful season triggered $225,000 worth of bonuses[13] for Holgorsen – $100,000 for a 10-win season, $75,000 for a BCS appearance and $50,000 for a BCS win.

In August 2012, Holgorsen received a new six-year contract. He will receive $2.3 million in the first year of the pact, with raises bringing his salary to $2.9 million at the end of the contract. He also is eligible for up to $600,000 in bonuses each year. The deal brings Holgorsen's compensation in line with other Big 12 coaches. In only his second year as a head coach, he ranks seventh in the 10-school conference in salary.[14]

Holgorsen has three children: McClayne, Logan and Karlyn.[15] He built his home in Morgantown in 2014. The home is the first luxury residence in the U.S. to be built completely of cross-laminated timber.[17]